Negative effects of ultrafine particle exposure during forced exercise on the expression of Brain-Derived Neurotrophic Factor in the hippocampus of rats

Neuroscience

Volumn 223, Issue , 2012, Pages 131-139

  Bos, I ^a,b   De Boever, P ^a,c   Int Panis, L ^a,c   Sarre, S ^b   Meeusen, R ^b  

^a FLEMISH INSTITUTE FOR TECHNOLOGICAL RESEARCH VITO   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

Author keywords

Air pollution; BDNF; Exercise; Olfactory bulb; Particulate matter; Prefrontal cortex

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

AIR POLLUTION; AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXERCISE; EXPOSURE; GENE; GENE EXPRESSION; HIPPOCAMPUS; INTERLEUKIN 1 ALPHA GENE; INTERLEUKIN 1 BETA GENE; INTERLEUKIN 6 GENE; MALE; NITRIC OXIDE SYNTHASE 2 GENE; NITRIC OXIDE SYNTHASE 3 GENE; NONHUMAN; NUCLEAR FACTOR ERYTHROID DERIVED 2 LIKE 2 GENE; OLFACTORY BULB; PARTICULATE MATTER; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR GENE; UPREGULATION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYTOKINES; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; RNA, MESSENGER; SILICONES;

EID: 84865558496     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.07.057     Document Type: Article

References (65)

1. Acikgoz O., Aksu I., Topcu A., Kayatekin B.M. Acute exhaustive exercise does not alter lipid peroxidation levels and antioxidant enzyme activities in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 2006, 406(1-2):148-151.
2. Adlard P.A., Perreau V.M., Engesser-Cesar C., Cotman C.W. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett 2004, 363(1):43-48.
3. Aguiar A.S., Castro A.A., Moreira E.L., Glaser V., Santos A.R., Tasca C.I., Latini A., Prediger R.D. Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 2011, 132(11-12):560-567.
4. Aksu I., Topcu A., Camsari U.M., Acikgoz O. Effect of acute and chronic exercise on oxidant-antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 2009, 452(3):281-285.
5. Ang E.T., Dawe G.S., Wong P.T., Moochhala S., Ng Y.K. Alterations in spatial learning and memory after forced exercise. Brain Res 2006, 1113(1):186-193.
6. Antunes H.K., Stella S.G., Santos R.F., Bueno O.F., de Mello M.T. Depression, anxiety and quality of life scores in seniors after an endurance exercise program. Rev Bras Psiquiatr 2005, 27(4):266-271.
7. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J Neuroimmunol 2004, 155(1-2):119-126.
8. Barrientos R.M. Voluntary exercise as an anti-neuroinflammatory therapeutic. Brain Behav Immun 2011, 25(6):1061-1062.
9. Bos I., Jacobs L., Nawrot T.S., de Geus B., Torfs R., Int Panis L., Degraeuwe B., Meeusen R. No exercise-induced increase in serum BDNF after cycling near a major traffic road. Neurosci Lett 2011, 500(2):129-132.
10. Block M.L., Calderon-Garciduenas L. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci 2009, 32:506-516.
11. Brook R.D., Rajagopalan S., Pope C.A., Brook J.R., Bhatnagar A., Diez-Roux A.V., Holguin F., Hong Y., Luepker R.V., Mittleman M.A., Peters A., Siscovick D., Smith S.C., Whitsel L., Kaufman J.D. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 2010, 121(21):2331-2378. American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism.
12. Calderón-Garcidueñas L., Solt A.C., Henríquez-Roldán C., Torres-Jardón R., Nuse B., Herritt L., Villarreal-Calderón R., Osnaya N., Stone I., García R., Brooks D.M., González-Maciel A., Reynoso-Robles R., Delgado-Chávez R., Reed W. Long-term air pollution is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid β-42 and α-synuclein in children and young adults. Toxicol Pathol 2008, 36(2):289-310.
13. Calderón-Garcidueñas L., et al. Air pollution, cognitive deficits and brain abnormalities: a pilot study with children and dogs. Brain Cogn 2008, 68(2):117-127.
14. Calderón-Garcidueñas L., Engle R., Mora-Tiscareño A., Styner M., Gómez-Garza G., Zhu H., Jewells V., Torres-Jardón R., Romero L., Monroy-Acosta M.E., Bryant C., González-González L.O., Medina-Cortina H., D'Angiulli A. Exposure to severe urban air pollution influences cognitive outcomes, brain volume and systemic inflammation in clinically healthy children. Brain Cogn 2011, 77(3):345-355.
15. Calderón-Garcidueñas L., Kavanaugh M., Block M., D'Angiulli A., Delgado-Chávez R., Torres-Jardón R., González-Maciel A., Reynoso-Robles R., Osnaya N., Villarreal-Calderon R., Guo R., Hua Z., Zhu H., Perry G., Diaz P. Neuroinflammation, hyperphosphorylated tau, diffuse amyloid plaques, and down-regulation of the cellular prion protein in air pollution exposed children and young adults. J Alzheimers Dis 2012, 28(1):93-107.
16. Campbell A., Oldham M., Becaria A., Bondy S.C., Meacher D., Sioutas C., Misra C., Mendez L.B., Kleinman M. Particulate matter in polluted air may increase biomarkers of inflammation in mouse brain. Neurotoxicology 2005, 26(1):133-140.
17. Campbell A., Araujo J.A., Li H., Sioutas C., Kleinman M. Particulate matter induced enhancement of inflammatory markers in the brains of apolipoprotein E knockout mice. J Nanosci Nanotechnol 2009, 9(8):5099-5104.
18. Chen J.C., Schwartz J. Neurobehavioral effects of ambient air pollution on cognitive performance in US adults. Neurotoxicology 2009, 30(2):231-239.
19. Cortese G.P., Barrientos R.M., Maier S.F., Patterson S.L. Aging and a peripheral immune challenge interact to reduce mature brain-derived neurotrophic factor and activation of TrkB, PLC{gamma}1, and ERK in hippocampal synaptoneurosomes. J Neurosci 2011, 31:4274-4279.
20. Dons E., Int Panis L., Van Poppel M., Theunis J., Willems H., Torfs R., Wets G. Impact of time-activity patterns on personal exposure to black carbon. Atmos Environ 2011, 10.1016/j.atmosenv.2011.03.064.
21. Ferris L.T., Williams J.S., Shen C.L. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc 2007, 39(4):728-734.
22. Funk J.A., Gohlke J., Kraft A.D., McPherson C.A., Collins J.B., Jean Harry G. Voluntary exercise protects hippocampal neurons from trimethyltin injury: possible role of interleukin-6 to modulate tumor necrosis factor receptor-mediated neurotoxicity. Brain Behav Immun 2011, 25(6):1063-1077.
23. Gerlofs-Nijland M.E., Boere A.J., Leseman D.L., Dormans J.A., Sandström T., Salonen R.O., van Bree L., Cassee F.R. Effects of particulate matter on the pulmonary and vascular system: time course in spontaneously hypertensive rats. Part Fibre Toxicol 2005, 2(1):2.
24. Goekint M., Roelands B., Heyman E., Njemini R., Meeusen R. Influence of citalopram and environmental temperature on exercise-induced changes in BDNF. Neurosci Lett 2011, 494(2):150-154.
25. Griesbach G.S., Gomez-Pinilla F., Hovda D.A. The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Res 2004, 1016(2):154-162.
26. Griesbach G.S., Hovda D.A., Molteni R., Wu A., Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience 2004, 125(1):129-139.
27. Griffin É.W., Mullally S., Foley C., Warmington S.A., O'Mara S.M., Kelly A.M. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 2011, 104(5):934-941.
28. Hartz A.M., Bauer B., Block M.L., Hong J.S., Miller D.S. Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the blood-brain barrier. FASEB J 2008, 22(8):2723-2733.
29. Huang A.M., Jen C.J., Chen H.F., Yu L., Kuo Y.M., Chen H.I. Compulsive exercise acutely upregulates rat hippocampal brain-derived neurotrophic factor. J Neural Transm 2006, 113(7):803-811.
30. Int Panis L., de Geus B., Vandenbulcke G., Willems H., Degraeuwe B., Bleux N., Mishra V., Thomas I., Meeusen R. Exposure to particulate matter in traffic: a comparison of cyclists and car passengers. Atmos Environ 2010, 44:2263-2270.
31. Jacobs L., Nawrot T.S., de Geus B., Meeusen R., Degraeuwe B., Bernard A., Sughis M., Nemery B., Int Panis L. Subclinical responses in healthy cyclists briefly exposed to traffic-related air pollution: an intervention study. Environ Health 2010, 9.
32. Janhall S., Jonsson A.M., Molnar P., Svensson E.A., Hallquist M. Size resolved traffic emission factors of submicrometer particles. Atmos Environ 2004, 38:4331-4340.
33. Janssen N.A., Hoek G., Simic-Lawson M., Fischer P., van Bree L., ten Brink H., Keuken M., Atkinson R.W., Anderson H.R., Brunekreef B., Cassee F.R. Black carbon as an additional indicator of the adverse health effects of airborne particles compared with PM10 and PM2.5. Environ Health Perspect 2011, 119(12):1691-1699.
34. Kwak M.K., Itoh K., Yamamoto M., Kensler T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol Cell Biol 2002, 22(9):2883-2892.
35. Leem Y.H., Lee Y.I., Son H.J., Lee S.H. Chronic exercise ameliorates the neuroinflammation in mice carrying NSE/htau23. Biochem Biophys Res Commun 2011, 406(3):359-365.
36. Levesque S., Surace M.J., McDonald J., Block M.L. Air pollution & the brain: subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease. J Neuroinflamm 2011, 8:105.
37. Masley S., Roetzheim R., Gualtieri T. Aerobic exercise enhances cognitive flexibility. J Clin Psychol Med Settings 2009, 16(2):186-193.
38. Mazzola P.N., Terra M., Rosa A.P., Mescka C.P., Moraes T.B., Piccoli B., Jacques C.E., Dalazen G., Cortes M.X., Coelho J., Dutra-Filho C.S. Regular exercise prevents oxidative stress in the brain of hyperphenylalaninemic rats. Metab Brain Dis 2011, 26(4):291-297.
39. MohanKumar S.M., Campbell A., Block M., Veronesi B. Particulate matter, oxidative stress and neurotoxicity. Neurotoxicology 2008, 29(3):479-488.
40. Nabkasorn C., Miyai N., Sootmongkol A., Junprasert S., Yamamoto H., Arita M., Miyashita K. Effects of physical exercise on depression, neuroendocrine stress hormones and physiological fitness in adolescent females with depressive symptoms. Eur J Public Health 2006, 16(2):179-184.
41. Nguyen T., Sherratt P.J., Huang H.C., Yang C.S., Pickett C.B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem 2003, 278(7):4536-4541.
42. Nguyen T., Yang C.S., Pickett C.B. The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 2004, 37(4):433-441.
43. Packer N., Pervaiz N., Hoffman-Goetz L. Does exercise protect from cognitive decline by altering brain cytokine and apoptotic protein levels? A systematic review of the literature. Exerc Immunol Rev 2010, 16:138-162.
44. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):e36.
45. Pfaffl M.W. Quantification strategies in real-time PCR. A-Z of quantitative PCR 2004, 87-112. International University Line (IUL), La Jolla, California. S.A. Bustin (Ed.).
46. Ranft U., Schikowski T., Sugiri D., Krutmann J., Krämer U. Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environ Res 2009, 109(8):1004-1011.
47. Rasmussen R. Quantification on the LightCycler. Rapid cycle real-time PCR methods and applications 2001, 21-34. Springer Press, Heidelberg. S. Meuer, C. Wittwer, K. Nakagawara (Eds.).
48. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., Secher N.H., Pedersen B.K., Pilegaard H. Evidence for a release of BDNF from the brain during exercise. Exp Physiol 2009, 94(10):1062-1069.
49. Rojas Vega S., Strüder H.K., Vera Wahrmann B., Schmidt A., Bloch W., Hollmann W. Acute BDNF and cortisol response to low intensity exercise and following ramp incremental exercise to exhaustion in humans. Brain Res 2006, 1121(1):59-65.
50. Salim S., Sarraj N., Taneja M., Saha K., Tejada-Simon M.V., Chugh G. Moderate treadmill exercise prevents oxidative stress-induced anxiety-like behavior in rats. Behav Brain Res 2010, 208(2):545-552.
51. Seaton A., MacNee W., Donaldson K., Godden D. Particulate air pollution and acute health effects. Lancet 1995, 345(8943):176-178.
52. Soya H., Nakamura T., Deocaris C.C., Kimpara A., Iimura M., Fujikawa T., Chang H., McEwen B.S., Nishijima T. BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 2007, 358(4):961-967.
53. Stroth S., Hille K., Spitzer M., Reinhardt R. Aerobic endurance exercise benefits memory and affect in young adults. Neuropsychol Rehabil 2009, 19(2):223-243.
54. Suglia S.F., Gryparis A., Wright R.O., Schwartz J., Wright R.J. Association of black carbon with cognition among children in a prospective birth cohort study. Am J Epidemiol 2008, 167(3):280-286.
55. Tuon T., Valvassori S.S., Lopes-Borges J., Fries G.R., Silva L.A., Kapczinski F., Quevedo J., Pinho R.A. Effects of moderate exercise on cigarette smoke exposure-induced hippocampal oxidative stress values and neurological behaviors in mice. Neurosci Lett 2010, 475(1):16-19.
56. Tin-Tin-Win-Shwe, Mitsushima D., Yamamoto S., Fukushima A., Funabashi T., Kobayashi T., Fujimaki H. Changes in neurotransmitter levels and proinflammatory cytokine mRNA expressions in the mice olfactory bulb following nanoparticle exposure. Toxicol Appl Pharmacol 2008, 226(2):192-198.
57. van Berlo D., Albrecht C., Knaapen A.M., Cassee F.R., Gerlofs-Nijland M.E., Kooter I.M., Palomero-Gallagher N., Bidmon H.J., van Schooten F.J., Krutmann J., Schins R.P. Comparative evaluation of the effects of short-term inhalation exposure to diesel engine exhaust on rat lung and brain. Arch Toxicol 2010, 84(7):553-562.
58. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3(7). Research 0034. 1-12.
59. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20(10):2580-2590.
60. Vaynman S., Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 2005, 19(4):283-295.
61. Vaynman S., Ying Z., Wu A., Gomez-Pinilla F. Coupling energy metabolism with a mechanism to support brain-derived neurotrophic factor-mediated synaptic plasticity. Neuroscience 2006, 139(4):1221-1234.
62. Vollert C., Zagaar M., Hovatta I., Taneja M., Vu A., Dao A., Levine A., Alkadhi K., Salim S. Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav Brain Res 2011, 224(2):233-240.
63. von Klot S., Cyrys J., Hoek G., Kühnel B., Pitz M., Kuhn U., Kuch B., Meisinger C., Hörmann A., Wichmann H.E., Peters A. Estimated personal soot exposure is associated with acute myocardial infarction onset in a case-crossover study. Prog Cardiovasc Dis 2011, 53(5):361-368.
64. Wu A., Ying Z., Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur J Neurosci 2004, 19(7):1699-1707.
65. Zahoransky R, Kerzenmacher S, Benali G, Lavigne R, Kassab J, Henneke D, Laile E (2003) On-line particle emission analysis of the CAST burner using LPME. Retrieved from: http://www.sootgenerator.com/documents/Zahoransky.pdf.